Ecology of viruses in soils: Past, present and future perspectives

Figures & data

Table 1 Books, reviews and primer articles that deal with viruses/phages in the environment in relation to the topics of this review

Author(s)	Environment	Contents/Topics
Viruses and bacteriophages
Bradley (1967)		Ultrastructure of bacteriophages and bacteriocins with many photographs.
Ackermann and DuBow (1987a)		Taxonomy, occurrence, multiplication, lysogeny, description, application of bacteriophages.
Ackermann and DuBow (1987b)		Systematics and identification of bacteriophages.
Zillig et al. (1988)		Viruses of archaebacteria with many photographs.
Reiter et al. (1988)		Viruses of archaebacteria known to date.
Van Etten et al. (1991)		Biology and molecular biology of Chlorella and algal viruses, their transferase and nuclease.
Ackermann (1998)		Caudovirales, morphology, genomes, lifestyle, amino-acid sequence alignment.
Ackermann (2001)		List of phages according to morphology.
Van Regenmortel et al. (2000)		Virus taxonomy, classification and nomenclature of viruses. Seventh Report of the International Committee on Taxonomy of Viruses
Canchaya et al. (2003b)		Prophage genomics, coevolution of bacteria and phages, roles of phage genes in host adaptation.
Fauquet et al. (2005)		Virus taxonomy, classification and nomenclature of viruses. Eighth Report of the International Committee on Taxonomy of Viruses.
Coexistence of hosts and viruses
Alexander (1981)	Soil	Mechanisms of coexistence of hosts and viruses in natural ecosystems.
Lenski (1988)	Microcosm	Interactions between bacteria and virulent bacteriophages.
Ecology of soil bacteriophages. Adsorption of viruses on soil particles
Gerba et al. (1975)	Soil, groundwater	Fate of wastewater bacteria and viruses in soil.
Duboise et al. (1979)	Soil	Survival, adsorption, movement, factors affecting survival.
Seeley and Primrose (1982)	Natural environments	Concentration, isolation.
Keswick and Gerba (1980)	Soil, groundwater	Viruses in groundwater. Survival and migration of viruses in soils.
Lipson and Stotzky (1984a)	Soil	Mechanisms of virus adsorption to particulates.
Stotzky (1985)	Soil	Mechanisms of adhesion of bacteria and viruses to clay minerals.
Stotzky (1986)	Soil	Effects of clay minerals on microbes and their events. Surface interactions between clay minerals and viruses.
Lipson and Stotzky (1987)	Soil	Biological and abiological factors affecting viral adsorption on clay minerals.
Williams et al. (1987)	Soil	Detection, factors affecting survival, phage–host interaction.
Marsh and Wellington (1994)	Soil	Abundance, survival, impact on host populations, lysogeny, and roles in genetic interactions.
Holizontal gene transfer in soil
Stotzky (1989)	Soil	Transduction in soil, biological and physicochemical factors.
Stotzky et al. (1990)	Soil	Methods for studying bacterial gene transfer in soil by conjugation and transduction.
Stotzky et al. (1991)	Soil	Factors affecting the transfer of genetic information among microorganisms in soil.
Yin and Stotzky (1997)	Natural environments	Gene transfer among bacteria, factors affecting transduction.
Biogeochemical cycles
Fuhrman (1992)	Marine	Microbial food web, virus and dissolved organic matter release, viral infection of bacteria, bacterial dominance.
Fuhrman and Suttle (1993)	Marine	Abundance, diversity, fast life cycle, agent of microbial mortality, organic matter cycling.
Suttle (1994)	Aquatic	Viral roles in mortality in aquatic microbial communities.
Bratbak et al. (1994)	Marine	Viruses and microbial loop. Abundance, distribution, activity, regulation.
Wilhelm and Suttle (1999)	Marine	Viruses and nutrient cycles. Distribution, viral mortality.
Fuhrman (1999)	Marine	Abundance, activity, biogeochemical and ecological effects.
Viruses in aquatic environments
Kapuscinski and Mitchell (1980)	Marine	Inactivation of viruses in the sea.
Moebus (1987)	Marine	Abundance, distribution, viral life and marine environment.
Børsheim (1993)	Marine	Abundance, morphology, burst size, decay and inactivation, host specificity.
Proctor (1997)	Marine	Abundance, morphology, infection of phages to bacterial hosts with many photographs.
Wommack and Colwell (2000)	Aquatic	Viral abundance and environmental parameters in aquatic ecosystems. Aquatic food web and viruses. Viral infection and host community diversity.
Suttle (2000)	Aquatic	Cyanophages, taxonomy, morphology, diversity, abundance and distribution in environment, effect on cyanobacteria.
Paul et al. (2002)	Marine	Overview of phage ecology, use of phage genomics for marine ecology.
Mann (2003)	Aquatic	Cyanophages, characterization, phage–host interactions, genomics, evolutionary biology.
Chibani-Chennoufi et al. (2004)	Natural environments	Seasonal variation, phage genomics, infection, survival strategy.
Weinbauer and Rassoulzadegan (2004)	Aquatic	Microbial diversity and viruses, viral diversity, viral-mediated gene transfer.
Weinbauer (2004)	Aquatic, soil	Characterization, distribution, diversity, growth and survival in environments. Life cycles in environments. Roles in food web process and gene transfer.
Mann (2005)	Natural environments	Abundance, diversity, phage–host interaction.
Suttle (2005)	Marine	Roles in global geochemical cycles and preservation of genetic diversity.
Horizontal gene transfer in aquatic environments
Hendrix et al. (2000)	General	Evolution of viruses.
Boyd and Brüssow (2002)	General	Virulence genes, phage–bacterium interaction.
Canchaya et al. (2003a)	General	Transduction, lateral gene transfer.
Frost et al. (2005)	Natural environments	Phages as agents of gene transfer. Genomics of phages, plasmids and transposons.
Hambly and Suttle (2005)	Aquatic	Genetic exchange within phages, photosynthetic genes, metagenomics.
Edwards and Rohwer (2005)	General	Importance of metagenomics in virus ecology.
Paul and Sullivan (2005)	Marine	Comparative phage genomics, photosynthetic genes, metagenomics.

Table 2 Soil, environmental and viral factors affecting the adsorption of viruses to soils

Factors	References
Type of clay minerals	Carlson et al. (1968); Lipson and Stotzky (1983, 1984b); Moore et al. (1981); Schiffenbauer and Stotzky (1982); Stotzky et al. (1981); Sykes and Williams (1978); Vettori et al. (1999)
Cation exchange capacity	Burge and Enkiri (1978); Lipson and Stotzky (1983); Moore et al. (1982); Schiffenbauer and Stotzky (1982); Stotzky et al. (1981)
Soil-associated and dissolved organic matter	Burge and Enkiri (1978); Carlson et al. (1968); Lipson and Stotzky (1984b); Moore et al. (1981; 1982); Stotzky et al. (1981); Zhuang and Jin (2003a)
Soil pH	Burge and Enkiri (1978); Gerba et al. (1975); Loveland et al. (1996); Pantastico-Caldas et al. (1992); Taylor et al. (1981)
Ionic strength and its constituent	Carlson et al. (1968); Lance and Gerba (1984); Lipson and Stotzky (1983); Stotzky et al. (1981); Zhuang and Jin (2003b)
Type of virus	Dowd et al. (1998); Goyal and Gerba (1979); Lipson and Stotzky (1985b); Meschke and Sobsey (2003); Moore et al. (1981); Schiffenbauer and Stotzky (1982); Stotzky et al. (1981); Zhuang and Jin (2003a, 2003b)

Table 3 Studies on temporal and spatial variations of viral abundance

Factors	References
Hours	Clokie et al. (2006a); Hennes and Suttle (1995); Jiang and Paul (1994); Weinbauer et al. (1995)
Days	Bratbak et al. (1990); Hennes and Simon (1995); Maranger et al. (1994)
Months	Cochran and Paul (1998); Hennes and Simon (1995); Jiang and Paul (1994); Mathias et al. (1995); Millard and Mann (2006); Nakayama et al. (2007a); Tapper and Hicks (1998); Weinbauer et al. (1993; 1995); Wilcox and Fuhrman (1994)
Years	Mathias et al. (1995); Weinbauer et al. (1993)
Depth
From oxic surface to anoxic deep waters	Boehme et al. (1993); Cochlan et al. (1993); Drake et al. (1998); Hara et al. (1991; 1996); Marie et al. (1999); Pina et al. (1998); Weinbauer and Höfle (1998)
Transect
Freshwater	Maranger and Bird (1995)
Estuarine	Wommack et al. (1992)
Coastal ocean	Boehme et al. (1993); Hennes and Suttle (1995); Steward et al. (1996); Weinbauer et al. (1993)
Open sea	Hara et al. (1996)

Figure 1  Pelagic food chain model and virus-mediated carbon flow (Weinbauer 2004). The dotted lines show virus-mediated pathways. All values are based on the flux of carbon fixed by primary producers (100%).

Table 4 Size distribution (%) of viral communities in various aquatic environments

Size range (nm)	< 30	30–60	60–80	80–100	> 100	Variables	References
Near shore
Chesapeake Bay	0	40	25	25	10	Once	Bergh et al. (1989)
Raunefjord	0	40–62	23–30	8–25	10–12	Seasonal variation	Bergh et al. (1989)
Raunefjord	0	33–44	22–26	22	9–22	Nine times within a month	Bratbak et al. (1990)
S. California Bight	0–58	0–77	0–63	0–13	0–4	Location	Cochlan et al. (1993)
Gulf of Bothnia	2–52	37–82	4–22	0–18	0–3	Location	Cochlan et al. (1993)
N. Adriatic Sea	5–6	50–76	14–26	4–12	1–8	Location, yearly	Weinbauer et al. (1993)
Alboran Sea	0	73	27	0	0	Location	Alonso et al. (2001)
Oyster pond	64–90		0–23	3–13	2–9	Monthly	Montaniéet al. (2002)
Open ocean
North Atlantic	0	33–69	27–33	1–33	2	Once	Bergh et al. (1989)
S. California Bight	0–26	21–80	11–51	1–8	0–2	Location	Cochlan et al. (1993)
Limnetic
Danube backwater	–	13–18	41–42 (60–90 nm), 41–45 (> 90 nm)			No seasonal variation	Mathias et al. (1995)
Danube River	74 (< 60 nm)		20 (60–90 nm)		6 (> 90 nm)	Monthly	Fischer and Velimirov (2002)
Lake Plußsee	0	65	17	14	3	Once	Bergh et al. (1989)
Lake Superior	53	45	2 (> 60 nm)			No seasonal variation	Tapper and Hicks (1998)
Floodwater of paddy fields
No Fertilizer plot	0–10	30–58	20–40	4–22	2–16	No seasonal variation	Nakayama et al. (2007b)
Chemical NPK plot	0–10	18–70	12–48	6–28	0–6	No seasonal variation	Nakayama et al. (2007b)
Chemical NPK+Ca plot	0–8	44–56	22–56	4–24	0–6	No seasonal variation	Nakayama et al. (2007b)
Compost plot	0	32–70	20–48	4–22	0–8	No seasonal variation	Nakayama et al. (2007b)

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